About
The Journal "Obstetrics and Gynecology"Journal HistoryAims and ScopePolicies on Conflict of Interest, Human and Animal Rights, and Informed ConsentEditorial ProcessData sharing statementAdvertising PolicyThe Process for Handling Cases Requiring Corrections, Retractions, and Editorial Expressions of ConcernEditorial BoardEditorial CounsilInformation for ProfessionalsNewsContacts
ArchiveEthical StandardsSubscription
For authors
InstructionsInformed consent policyContract offerEASE GuidelinesICJME CriteriaWAME Recommendations on ChatGPT and Chatbots in Relation to Scholarly Publications
Reviewing
About
The Journal "Obstetrics and Gynecology"Journal HistoryAims and ScopePolicies on Conflict of Interest, Human and Animal Rights, and Informed ConsentEditorial ProcessData sharing statementAdvertising PolicyThe Process for Handling Cases Requiring Corrections, Retractions, and Editorial Expressions of ConcernEditorial BoardEditorial CounsilInformation for ProfessionalsNewsContacts
ArchiveEthical StandardsSubscription
For authors
InstructionsInformed consent policyContract offerEASE GuidelinesICJME CriteriaWAME Recommendations on ChatGPT and Chatbots in Relation to Scholarly Publications
Reviewing
Logout
Obstetrics and Gynegology2020№3
The role of gut microbiota...

The role of gut microbiota in the development of gestational diabetes mellitus

DOI
https://dx.doi.org/10.18565/aig.2020.3.18-24

Onopriychuk A.R., Kapustin R.V., Arzhanova O.N.

D.O. Ott Research Institute of Obstetrics, Gynecology, and Reproductology, Saint Petersburg, Russia
Gut microbiota regulates many processes occurring in the intestine, affecting its immune and endocrine functions, the absorption of substances. There is a hypothesis that intestinal dysbiosis plays a role in the pathogenesis of gestational diabetes mellitus (GDM). The paper reviews the data available in the literature of the world’s leading reference bases (MEDLINE, EMBASE, Cochrane) on changes in the microbiota and microbiome in women with GDM. An analysis of the findings has revealed numerous correlations between specific bacterial taxa and changes in the metabolic process in the body during pregnancy. The possible mechanism for the development of GDM is the occurrence of inflammation in the intestinal wall in the presence of gut dysbiosis, which results in barrier dysfunction of enterocytes and in an increase in their permeability and endotoxemia. This leads to overexpression of proinflammatory cytokines and increased insulin resistance. The use of probiotics is a method to correct gut dysbiosis. The administration of probiotics is shown to reduce subclinical inflammatory responses and to restore the balance of absorbed substances. It is probable that this method may also be relevant to the therapy of hyperglycemic states during pregnancy.

Keywords

microbiota
microbiome
microflora
gestational diabetes mellitus
insulin resistance
hyperglycemia
probiotics
Full text (in Russian)

References

  1. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2012; 35(Suppl. 1): S64–71. https:/dx.doi.org/10.2337/dc12-s064.
  2. International Diabetes Federation. IDF Diabetes Atlas, 8th ed. Brussels, Belgium: International Diabetes Federation; 2017.
  3. Schneider S., Hoeft B., Freerksen N., Fischer B., Roehrig S., Yamamoto S., Maul H. Neonatal complications and risk factors among women with gestational diabetes mellitus. Acta Obstet. Gynecol. Scand. 2011; 90(3): 231–7. https:/dx.doi.org/10.1111/j.1600-0412.2010.01040.x.
  4. Qin J., Li Y., Cai Z., Li S., Zhu J., Zhang F. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012; 490(7418): 55–60. https:/dx.doi.org/10.1038/nature11450.
  5. Karlsson F.H., Tremaroli V., Nookaew I., Bergstrom G., Behre C.J., Fagerberg B., et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013; 498(7452): 99–103. https:/dx.doi.org/10.1038/nature12198.
  6. Cani P.D., Neyrinck A.M., Fava F., Knauf C., Burcelin R.G., Tuohy K.M. et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. 2007; 50(11): 2374–83. https:/dx.doi.org/10.1007/s00125-007-0791-0.
  7. Pedersen H.K., Gudmundsdottir V., Nielsen H.B., Hyotylainen T., Nielsen T., Jensen B.A. et al. Human gut microbes impact host serum metabolome and insulin sensitivity. Nature. 2016; 535(7612): 376–81. https:/dx.doi.org/10.1038/nature18646.
  8. Koren O., Goodrich J.K., Cullender T.C., Spor A., Laitinen K., Bäckhed H.K., et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012; 150(3): 470–80. https:/dx.doi.org/10.1016/j.cell.2012.07.008.
  9. Liu J., Yang H., Yin Z., Jiang X., Zhong H., Qiu D., et al. Remodeling of the gut microbiota and structural shifts in preeclampsia patients in South China. Eur. J. Clin. Microbiol. Infect. Dis. 2017; 36(4): 713–9. https:/dx.doi.org/10.1007/s10096-016-2853-z.
  10. Gomez-Arango L.F., Barrett H.L., Mcintyre H.D., Callaway L.K., Morrison M., Dekker Nitert M.; SPRING Trial Group. Connections between the gut microbiome and metabolic hormones in early pregnancy in overweight and obese women. Diabetes. 2016; 65(8): 2214–23. https:/dx.doi.org/10.2337/db16-0278.
  11. Капустин Р.В., Аржанова О.Н. Субклиническое воспаление как фактор развития инсулинорезистентности во время беременности. Российский вестник акушера-гинеколога. 2017; 17(1): 27–36. [Kapustin R.V., Arzhanova O.N. Subclinical inflammation as a factor for the development of insulin resistance during pregnancy. Russian Bulletin of Obstetrician-Gynecologist/Rossiyskiy vestnik akushera-ginekologa. 2017; 17(1): 27–36. (in Russian).].
  12. Wang J., Jia H. Metagenome-wide association studies: fine-mining the microbiome. Nat. Rev. Microbiol. 2016; 14(8): 508-22. https:/dx.doi.org/10.1038/nrmicro.2016.83.
  13. Turnbaugh P.J., Ley R.E., Mahowald M.A., Magrini V., Mardis E.R., Gordon J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006; 444(7122): 1027–31. https:/dx.doi.org/10.1038/nature05414.
  14. Rajilic Stojanovic M., Heilig H.G., Molenaar D., Kajander K., Surakka A., Smidt H., et al. Development and application of the human intestinal tract chip, a phylogenetic micro array: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ. Microbiol. 2009; 11(7): 1736–51. https:/dx.doi.org/10.1111/j.1462–2920.2009.01900.x.
  15. Naik S., Bouladoux N., Wilhelm C., Molloy M.J., Salcedo R., Kastenmuller W. et al. Compartmentalized control of skin immunity by resident commensals. Science. 2012; 337(6098): 1115–9. https:/dx.doi.org/10.1126/science.1225152.
  16. Qin J., Li R., Raes J., Arumugam M., Burgdorf K.S., Manichanh C. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010; 464(7285): 59-65.
  17. Backhed F., Ding H., Wang T., Hooper L.V., Koh G.Y., Nagy A. et al. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA. 2004; 101(44): 15718–23. https:/dx.doi.org/10.1073/pnas.0407076101.
  18. Ley R.E., Backhed F., Turnbaugh P., Lozupone C.A., Knight R.D., Gordon J.I. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA. 2005; 102(31): 11070-5. https:/dx.doi.org/10.1073/pnas.0504978102.
  19. Girdwood R.H. The possible effects of gastro-intestinal bacteria on the absorption of Vitamin B12. Rev. Hematol. 1955; 10(2): 187–93. discussion, 207–11.
  20. Everard A., Cani P.D. Gut microbiota and GLP-1. Rev. Endocr. Metab. Disord. 2014; 15(3): 189–96. https:/dx.doi.org/10.1007/s11154-014-9288-6.
  21. Ploger S., Stumpff F., Penner G.B., Schulzke J.D., Gabel G., Martens H. et al.Microbial butyrate and its role for barrier function in the gastrointestinal tract. Ann. N.Y. Acad. Sci. 2012; 1258: 52–9. https:/dx.doi.org/10.1111/j.1749-6632.2012.06553.x.
  22. Kau A.L., Ahern P.P., Griffin N.W., Goodman A.L., Gordon J.I. Human nutrition, the gut microbiome and the immune system. Nature. 2011; 474(7351): 327–36. https:/dx.doi.org/10.1038/nature10213.
  23. Clarke G., Stilling R.M., Kennedy P.J., Stanton C., Cryan J.F., Dinan T.G. Minireview: Gut microbiota: The neglected endocrine organ. Mol. Endocrinol. 2014; 28(8): 1221–38. https:/dx.doi.org/10.1210/me.2014-1108.
  24. Meijnikman A.S., Gerdes V.E., Nieuwdorp M., Herrema H. Evaluating causality of gut microbiota in obesity and diabetes in humans. Endocr. Rev. 2018; 39(2): 133–53. https:/dx.doi.org/0.1210/er.2017-00192.
  25. Sircana A., Framarin L., Leone N., Berrutti M., Castellino F., Parente R. et al.Altered gut microbiota in type 2 diabetes: Just a coincidence? Curr. Diab. Rep. 2018; 18(10): 98. https:/dx.doi.org/10.1007/s11892-018-1057-6.
  26. Hu C., Wong F.S., Wen L. Type 1 diabetes and gut microbiota: Friend or foe? Pharmacol. Res. 2015; 98: 9–15. https:/dx.doi.org/10.1016/j.phrs.2015.02.006.
  27. Caricilli A.M., Saad M.J. The role of gut microbiota on insulin resistance. Nutrients. 2013; 5(3): 829–51. https:/dx.doi.org/10.3390/nu5030829.
  28. Collado M.C., Isolauri E., Laitinen K. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am. J. Clin. Nutr. 2008; 88(4): 894–9. https:/dx.doi.org/10.1093/ajcn/88.4.894.
  29. Haro C., Garcia-Carpintero S., Alcala-Diaz J.F., Gomez-Delgado F., Delgado-Lista J., Perez-Martinez P. et al. The gut microbial community in metabolic syndrome patients is modified by diet. J. Nutr. Biochem. 2016; Jan. 27: 27–31. https:/dx.doi.org/10.1016/j.jnutbio.2015.08.011.
  30. Gohir W., Whelan F.J., Surette M.G., Moore C., Schertzer J.D., Sloboda D.M. Pregnancy-related changes in the maternal gut microbiota are dependent upon the mother’s periconceptional diet. Gut Microbes. 2015; 6(5): 310–20.https:/dx.doi.org/10.1080/19490976.2015.1086056.
  31. Mueller N.T., Shin H., Pizoni A., Werlang I.C., Matte U., Goldani M.Z. et al. Birth mode-dependent association between pre-pregnancy maternal weight status and the neonatal intestinal microbiome. Sci. Rep. 2016; 6: 23133.https:/dx.doi.org/10.1038/srep23133.
  32. Natarajan N., Pluznick J.L. From microbe to man: the role of microbial short chain fatty acid metabolites in host cell biology. Am J Physiol. Cell Physiol. 2014; 307(11): C979-85. https:/dx.doi.org/10.1152/ajpcell.00228.2014.
  33. Brun P., Castagliuolo I., Di Leo V., Buda A., Pinzani M., Palù G., Martines D. Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2007; 292(2): G518–25. https:/dx.doi.org/10.1152/ajpgi.00024.2006.
  34. Lin H.V., Frassetto A., Kowalik E.J. Jr, Nawrocki A.R., Lu M.M., Kosinski J.R. et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One. 2012; 7(4): e35240. https:/dx.doi.org/10.1371/journal.pone.0035240.
  35. Cani P.D., Amar J., Iglesias M.A., Poggi M., Knauf C., Bastelica D. et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007; 56(7): 1761–72. https:/dx.doi.org/10.2337/db06-1491.
  36. Asemi Z., Samimi M., Tabassi Z., Naghibi Rad M., Rahimi Foroushani A., Khorammian H., Esmaillzadeh A. Effect of daily consumption of probiotic yoghurt on insulin resistance in pregnant women: a randomized controlled trial. Eur J Clin Nutr. 2013; 67(1): 71–4. https:/dx.doi.org/10.1038/ejcn.2012.189.
  37. Tolhurst G., Heffron H., Lam Y.S., Parker H.E., Habib A.M., Diakogiannaki E. et al. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes. 2012; 61(2): 364–71.https:/dx.doi.org/10.2337/db11-1019.
  38. Kuang Y.S., Lu J.H., Li S.H., Li J.H., Yuan M.Y., He J.R. et al. Connections between the human gut microbiome and gestational diabetes mellitus. Gigascience. 2017; 6(8): 1–12. https:/dx.doi.org/10.1093/gigascience/gix058.
  39. Manco M., Putignani L., Bottazzo G.F. Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr. Rev. 2010; 31(6): 817–44. https:/dx.doi.org/10.1210/er.2009-0030.
  40. Abreu M.T. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol. 2010; 10(2): 131–44. https:/dx.doi.org/10.1038/nri2707.
  41. Buchanan T.A., Xiang A.H., Page K.A. Gestational diabetes mellitus: risks and management during and after pregnancy. Nat. Rev. Endocrinol. 2012; 8(11): 639–49. https:/dx.doi.org/10.1038/nrendo.2012.96.
  42. Kim Y.A., Keogh J.B., Clifton P.M. Probiotics, prebiotics, synbiotics and insulin sensitivity. Nutr Res Rev. 2018; 31(1): 35–51. https:/dx.doi.org/10.1017/S095442241700018X.
  43. Guo Z., Liu X.M., Zhang Q.X., Shen Z., Tian F.W., Zhang H., et al. Influence of consumption of probiotics on the plasma lipid profile: a meta-analysis of randomised controlled trials. Nutr. Metab. Cardiovasc. Dis. 2011; 21(11): 844–50. https:/dx.doi.org/10.1016/j.numecd.2011.04.008.
  44. DeWeerdt S. How baby’s first microbes could be crucial to future health. Nature. 2018; 555(7695): S18–9. https:/dx.doi.org/10.1038/d41586-018-02480-6.
  45. Sanchez B., De Los Reyes-Gavilan C.G., Margolles A., Gueimonde M. Probiotic fermented milks: present and future. Int. J. Dairy Technol. 2009; 62: 472–83. https:/dx.doi.org/10.1111/j.1471-0307.2009.00528.x.
  46. Hill C., Guarner F., Reid G., Gibson G.R., Merenstein D.J., Pot B., et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014; 11(8): 506-14.https:/dx.doi.org/10.1038/nrgastro.2014.66.
  47. Griffin C. Probiotics in obstetrics and gynaecology. Aust. N. Z. J. Obstet. Gynaecol. 2015; 55(3): 201–9. https:/dx.doi.org/10.1111/ajo.12303.
  48. Palaria A., Johnson-Kanda I., O’Sullivan D.J. Effect of a synbiotic yogurt on levels of fecal bifidobacteria, clostridia, and enterobacteria. Appl. Environ. Microbiol. 2012; 78(4): 933–40. https:/dx.doi.org/10.1128/AEM.05848-11.
  49. Rogozinska E., Chamillard M., Hitman G.A., Khan K.S., Thangaratinam S. Nutritional manipulation for the primary prevention of gestational diabetes mellitus: a meta-analysis of randomised studies. PLoS One. 2015; 10(2): e0115526. https:/dx.doi.org/10.1371/journal.pone.0115526.
  50. Laitinen K., Poussa T., Isolauri E. Probiotics and dietary counselling contribute to glucose regulation during and after pregnancy: a randomised controlled trial. Br. J. Nutr. 2009; 101(11): 1679–87. https:/dx.doi.org/10.1017/S0007114508111461.
  51. Lindsay K.L., Kennelly M., Culliton M., Smith T., Maguire O.C., Shanahan F. et al. Probiotics in obese pregnancy do not reduce maternal fasting glucose: a double-blind, placebo-controlled, randomized trial (Probiotics in Pregnancy Study). Am. J. Clin. Nutr. 2014; 99(6): 1432–9. https:/dx.doi.org/10.3945/ajcn.113.079723.
  52. Lindsay K.L., Brennan L., Kennelly M.A., Maguire O.C., Smith T., Curran S. et al. Impact of probiotics in women with gestational diabetes mellitus on metabolic health: a randomized controlled trial. Am. J. Obstet. Gynecol. 2015; 212(4): 496. e1–11. https:/dx.doi.org/10.1016/j.ajog.2015.02.008.
  53. Dolatkhah N., Hajifaraji M., Abbasalizadeh F., Aghamohammadzadeh N., Mehrabi Y., Abbasi M. Is there a value for probiotic supplements in gestational diabetes mellitus? A randomized clinical trial. J. Health Popul. Nutr. 2015; 33: 25. https:/dx.doi.org/10.1186/s41043-015-0034-9.
  54. Serino M., Fernández-Real J.M., García-Fuentes E., Queipo-Ortuño M., Moreno-Navarrete J.M., Sánchez A., et al. The gut microbiota profile is associated with insulin action in humans. Acta Diabetol. 2013; 50(5): 753–61.https:/dx.doi.org/10.1007/s00592-012-0410-5.

Received 10.11.2019

Accepted 29.11.2019

About the Authors

Alexandra R. Onopriychuk, Junior Researcher, Department of Obstetrics and Perinatology, D.O. Ott Research Institute of Obstetrics, Gynecology, and Reproductology.
Tel.: +7(921)7701055. Email: alexandraonopriychuk@gmail.com; ORCID ID 0000-0002-3332-4920
Roman V. Kapustin, Candidate of Medical Sciences, Scientific Secretary of the D.O. Ott Research Institute of Obstetrics, Gynecology, and Reproductology.
Tel.: +7 (911)0890769. Email: kapustin.roman@gmail.com
Olga N. Arzhanova, MD, professor; Leading Researcher, Department of Obstetrics and Perinatology, D.O. Ott Research Institute of Obstetrics, Gynecology, and Reproductology. Tel.: +7 (921)9379536. E-mail: arjanova_olga@mail.ru

For citation: Onopriychuk A.R., Kapustin R.V., Arzhanova O.N. The role of gut microbiota in the development of gestational diabetes mellitus.
Akusherstvo i Ginekologiya/ Obstetrics and gynecology. 2020; 3: 18-24. (In Russian).
https://dx.doi.org/10.18565/aig.2020.3.18-24

Similar Articles

№11 / 2023
Tyutyunnik V.L., Kan N.E., Tezikov Yu.V., Lipatov I.S., Mikhailova O.I., Mirzabekova D.D.
Complex therapy of recurrent vulvovaginal candidiasis in pregnancy
№4 / 2024
Tezikov Yu.V., Lipatov I.S., Tyutyunnik V.L., Kan N.E., Kurbanova A.M.
The concept of epigenetic modifications in fetal metabolic programming
№10 / 2024
Zalozniaia I.V., Kopteeva E.V., Milyutina Yu.P., Korenevsky A.V., Arutjunyan A.V., Shelaeva E.V., Kapustin R.V., Kogan I.Yu.
The levels of oxidative stress markers in maternal and umbilical cord blood of pregnant women with diabetes mellitus in terms of blood flow redistribution in the fetal venous system
№12 / 2023
Apolikhina I.A., Teterina T.A., Tarnaeva L.A., Bartous K.A.H.
Women's and men's health through the prism of the International Federation of Gynaecology and Obstetrics 2023 recommendations. A new insight into the microbiome and intimate hygiene
№8 / 2024
Baranouskaya A.I., Voronetsky A.N.
Critical analysis of the current data on the normal endometrial microbiome
By continuing to use our site, you consent to the processing of cookies that ensure the proper functioning of the site.